His full name was Oscar-Arthur Honegger, but his first name was never used. He studied harmony and violin in Paris until his parents moved to Zürich, Switzerland, when he studied at the Conservatory there. He then went back to Paris to study with Charles-Marie Widor and Vincent d'Indy. He wrote a balletLe dit des jeux du monde in 1918. In 1926 he married Andrée Vaurabourg, a pianist and fellow student at the Paris Conservatoire. They often went on tour together, and his wife played the piano parts to his compositions. The couple had one daughter, Pascale, born in 1932. Honegger also had a son, Jean-Claude (1926-2003) whose mother was the singer Claire Croiza.

In the early 1920s Honegger became famous with the "dramatic psalm" "Le Roi David" ("King David"), which is still often sung by choirs. He wrote a lot of music between the wars, including the oratorioJeanne d'Arc au bûcher, one of his best works. It tells the story of Joan of Arc.

Honegger loved trains. As a student he had spent some time travelling to Paris twice a week by train from Le Havre. His popular orchestral work Pacific 231 describes a train on the Canadian Pacific Railway. It was an early piece, written in 1923.

In 1947 Honegger suffered a severe heart attack, and after that he composed little. A second heart attack caused his death eight years later in Paris.